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Home , Diffuse axonal injury, Spinal cord injury, Traumatic brain injury

J Rehabil Med 2007; 39: 622–626

ORIGINAL REPORT

TRAUMATIC IS UNDER-DIAGNOSED IN WITH INJURY

Anu Tolonen, LicPsych1, Jukka Turkka, MD, PhD1, Oili Salonen, MD, PhD2, Eija Ahoniemi, MD1 and Hannu Alaranta, MD, PhD1 From the 1Käpylä Rehabilitation Centre, Finnish Association of People with Mobility , and 2Department of Radiology, Helsinki University Hospital, Helsinki, Finland

Objective: To investigate the occurrence and severity of trau- bilitation, vocational and psychosocial survival of matic brain injury in patients with traumatic spinal cord patients with SCI (2–7). After SCI, or injury. alone represents the onset of a massive change in the life of Design: Cross-sectional study with prospective neurological, any individual. In addition, most patients with SCI experience neuropsychological and neuroradiological examinations and medical problems, including neurogenic bladder and bowel, retrospective medical record review. loss of sensation, , , sexual dysfunction and Patients: Thirty-one consecutive, traumatic spinal cord in- skin problems. However, from the perspectives of vocational jury patients on their first post- rehabilitation period planning, supportive interventions and psychosocial outcome, in a national rehabilitation centre. concomitant TBI is a central factor to be considered. Methods: The American Congress of Rehabilitation Medi- TBI produces marked disturbances in cognitive and emo- cine diagnostic criteria for mild were tional functioning, e.g. fatigue, problems in , con- applied. Assessments were performed with neurological and centration, , and judgement, irritability, emotional neuropsychological examinations and magnetic resonance lability, and acting in socially inappropriate ways. Patients imaging 1.5T. Results: Twenty-three of the 31 patients with spinal cord in- with SCI with concomitant TBI are at risk for a complicated jury (74%) met the diagnostic criteria for traumatic brain rehabilitation process and unfavourable outcome if TBI is not injury. Nineteen patients had sustained a loss of conscious- recognized and the rehabilitation approach modified. ness or post-traumatic . Four patients had a focal In SCI, because the enormous physical injury is a focus of con- neurological finding and 21 had neuropsychological findings cern, the basic indicators of TBI, including loss of apparently due to traumatic brain injury. Trauma-related (LOC), post-traumatic amnesia (PTA), neurological symptoms magnetic resonance imaging abnormalities were detected in and signs due to TBI, and neurobehavioural changes, may go 10 patients. Traumatic brain injury was classified as moder- undetected and undocumented. Furthermore, patients with a ate or severe in 17 patients and mild in 6 patients. Glasgow Score (GCS) (8) of 13–15 may also suffer from Conclusion: The results suggest a high frequency of trau- severe TBI (9), and often structural damage cannot be detected in matic brain injury in patients with traumatic spinal cord conventional neuroradiological examinations, such as magnetic injury, and stress a special diagnostic issue to be considered resonance imaging (MRI) despite brain injury (10, 11). Altered in this group. mental status, e.g. fatigue, information processing problems, and Key words: traumatic brain injury, , co-occur- changes in behavioural and emotional regulation, can be misin- rence, rehabilitation. terpreted as post-anaesthesial sequelae, effects of medication, or J Rehabil Med 2007; 39: 622–626 a psychological reaction to a massive life change. In the systematic studies examining the co-occurrence of Correspondence address: Anu Tolonen, Käpylä Reha- TBI in traumatic SCI, the was estimated to be bilitation Centre, PO Box 103, FI-00251 Helsinki, Finland. 40–60% (2–7). However, only 1 or 2 indicators (LOC, PTA, E-mail: [email protected] neuropsychological deficits) have been used when diagnosing Submitted September 13, 2006; accepted April 19, 2007. TBI. Previous studies have not combined neurological, neuro­ psychological and neuroradiological methods in evaluating the occurrence and severity of TBI within a SCI population. INTRODUCTION The aim of this study was to investigate the occurrence and severity of TBI by using neurological, neuropsychological and Traumatic spinal cord (SCI) typically result from neuroradiological examinations in patients with traumatic SCI high kinetic accidents such as falls or traffic accidents. As admitted to the rehabilitation centre. traumatic brain injury (TBI) occurs in similar circumstances, these neurotraumas can frequently be assumed to be present concomitantly. In fact, most cervical SCIs are secondary to METHODS indirect forces transmitted to the spine through the head (1). The study was carried out between April 2000 and September 2001 at TBI has been suggested to be a major concern in the reha- the Käpylä Rehabilitation Centre, Helsinki, Finland, according to the

J Rehabil Med 39 © 2007 Foundation of Rehabilitation Information. ISSN 1650-1977 doi: 10.2340/16501977-0101 TBI in patients with SCI 623 principles of the Declaration of Helsinki and with the approval of the local Table I. Classification of patients according to spinal cord injury and ethics committees. Informed consent was obtained from all patients. American Spinal Injury Association (ASIA) Impairment Scale (AIS) There are no data on the actual of traumatic SCI in Finland. More than 90% of all patients with traumatic SCI with paraplegia or AIS tetraplegia in Finland are referred to the Käpylä Rehabilitation Centre A B C D Total upon conclusion of the acute phase. The incidence of referred patients Tetraplegia 3 4 7 2 16 is 1.1/100,000 inhabitants per year. Paraplegia 9 2 3 1 15 Total 12 6 10 3 31 Patients Thirty-one (1 female and 30 males, mean age 36 years) of 80 consecu- A: Complete: no motor or sensory function is preserved in the sacral tive patients with traumatic SCI on the first post-acute rehabilitation segments S4–S5. period fulfilled the following inclusion criteria: (i) age 16–54 years; B: Incomplete: sensory but not motor function is preserved below the (ii) no history of prolonged or ; and (iii) no neurological level and includes the sacral segments S4–S5. history of psychiatric or cerebral disorder including TBI. Because the C: Incomplete: motor function is preserved below the neurological battery is appropriate only for adults over 16 level, and more than half of key muscles below the neurological level years of age, younger patients were not studied. Also, the patients over have a muscle grade less than 3. 54 years of age were excluded because age-related non-specific changes D: Incomplete: motor function is preserved below the neurological may confound the MRI interpretation. The exclusion criteria (ii) and (iii) level, and at least half of key muscles below the neurological have a were used to ensure that neuropsychological and neurological examina- muscle grade of 3 or more. tions did not reflect these possibly pre-existing conditions. Forty-nine of the original 80 patients were excluded for the follow- ing reasons: age under 16 years or over 54 years (n = 26), prolonged Neurological examinations alcohol or substance abuse (n = 11), psychiatric disorder (n = 3), The was performed by the neurologist (JT), previous cerebral disorder (n = 1), insufficient knowledge of Finnish who was unaware of the results of neuroradiological and neuropsy- or Swedish (n = 4), refusal (n = 2), rehabilitation period too short chological examinations. This examination included an evaluation (n = 1) and Hallowest not suitable for MRI (n = 1). of any neurological symptoms and signs due to TBI, such as cranial The mean period of education of the patients was 12 (range 8–16) dysfunction, pyramidal and extrapyramidal signs, sensory hemi- years. SCIs were caused by traffic accidents (n = 14; 46%), falls syndrome, and cerebellar signs based on medical records, patients’ (n = 13; 42%), diving accidents (n = 2; 6%), and other causes (n = 2; history and clinical examination. The routine pattern of examination 6%). Twelve patients had complete lesions of the spinal cord according comprised sensory evaluation, muscle tone and power measurements to the impairment scale by American Spinal Injury Association (ASIA) in the upper extremities of patients with paraplegia, and deep tendon (12, 13). Patients’ spinal cord injuries are presented in Table I. reflex and finger-to-nose testing. GCS at the time of injury or at admis- sion and any alteration of consciousness after the injury were evalu- TBI diagnostic criteria ated retrospectively from the medical documents by the neurologist. The diagnostic criteria for mild TBI diagnostics by the American Also, secondary brain injuries and other complications affecting brain Congress of Rehabilitation Medicine (14) were applied (Table II). function, such as , massive bleeding and medications, were The criteria include any of the following: (i) any period of LOC; (ii) evaluated by the same neurologist. The neurological examinations any PTA; (iii) any alteration in mental state; and (iv) any focal neuro- were performed 17.8 weeks (mean; standard deviation (SD) 11.5) after logical finding (transient or permanent) due to TBI. To ascertain that the injury. The ASIA impairment scale (12, 13) was performed by the all the patients with TBI were detected, we added to the diagnostic physiatrist (EA) at the beginning of the rehabilitation period. criteria neuropsychological finding due to TBI in the study phase and neuroradiological finding due to TBI during either the acute phase or Neuroradiological examination the study phase. MRI was performed 20.6 weeks (mean; SD 10.8) after the injury and To investigate these criteria, patients underwent neurological, neuro­ evaluated by the neuroradiologist (OS), who was unaware of the results radiological and neuropsychological examinations. The diagnostic of neurological and neuropsychological examinations. The examinations finding was excluded from the analysis if there was any confounding were performed with a Siemens Vision imager (Erlangen, Germany) factor, e.g. intoxication, hypoxia, medication or other medical condi- operating at 1.5 T. Axial scans with T2 TSE, FLAIR, and T2* gradient tion affecting brain function and cognition. echo sequences were obtained. Also obtained were T2 TSE coronal and

Table II. Diagnostic criteria for classification of traumatic brain injury (TBI) severity Diagnostic criteria Mild Moderate Severe Altered level or loss of consciousness GCS 13–15 and/or GCS 9–12 and/or GCS 3–8 and/or any LOC < 30 min LOC > 30 min – 6 h LOC > 6 h PTA Any PTA < 24 h 24 h – 7 days > 7 days Neurological finding due to TBI No findings Transient neurological finding Permanent neurological (symptom) finding (sign) Neuroradiological finding due to TBI No findings Neuroradiological TBI finding Neuroradiological TBI finding and neurosurgical operation Neuropsychological finding due to TBI No neuropsychological findings in tests 1–2 SD* in tests or > 2 SD* in tests or unable but subjective symptoms with predictable limited capability in work but to work and permanent normal work and ADL performance normal ADL difficulties in ADL *Worse than the normal mean in one or more neuropsychological tests. LOC: loss of consciousness; GCS: Glasgow Coma Score; PTA: post-traumatic amnesia; ADL: activities of daily living; SD: standard deviation.

J Rehabil Med 39 624 A. Tolonen et al.

T1 3D MPRAGE sagittal slices. Non-specific high signal foci were ex- Digit Span and Similarities) of the Wechsler Adult Intelligence Scale cluded from the analysis, only contusions and post-hemorrhagic lesions Revised (WAIS‑R) (15) were used. A computerized version of the with typical location to were included. Paced Auditory Serial Addition Test (PASAT) (16) was applied for testing attention. Memory functions were evaluated by using the Visual Pairs subtest from the Wechsler Memory Scale Revised (WMS‑R) (17), Neuropsychological examination the Buschke‑Fuld Selective Reminding test (18) and Kalska’s Memory The neuropsychological examination was carried out by the clinical for Person Data, which is a modification of Cronholm’s and Molander’s neuropsychologist (AT), who was unaware of the results of neurologi- KS‑memory test. For studying behavioural, emotional and personal- cal and neuroradiological examinations. Three sub-tests (Arithmetic, ity changes, the Depression Scale (19, 20) and the Neurobehavioural

Table III. Traumatic brain injury (TBI) diagnostic findings Patients No./Age Neuropsycho- TBI (years) GCS Length of PTA Neurological finding Radiological finding logical finding diagnosis 1/36 15 16 h – – Severe Severe 2/19 CF 142 8 days CF non-specific finding Contusions at both sides of Moderate Severe cerebellum 3/32 CF 142 CF 2.5 days2, 5 – – Mild Mild 4/27 CF 142 CF 14 days2, 5, 6 – Haemorrhage, DAI Mild Moderate 5/46 15 2–3 min – CF non-specific high signal Mild Mild foci of 6/54 15 – CF non-specific finding CF non-specific high signal – No foci of white matter 7/24 15 5 min – – Severe Severe 8/48 15 CF 6 days5 – – – No 9/33 14 3 h CF 3–4 weeks5, 6 CF non-specific finding Right temporal contusion, Severe Severe DAI 10/37 14 12 h – – Mild Moderate 11/23 14 3 h, CF 3 weeks5 CF non-specific finding – Mild Mild 12/50 15 30 min – CF non-specific high signal – Mild foci of white matter 13/45 15 CF 12 hours2, 5 – – – No 14/37 15 60 min – – Moderate Moderate 15/35 CF 132 CF 7 days2, 5 – Traumatic subarachnoidal Mild Moderate haemorrhage 16/521 15 3 h – CF non-specific high signal – Mild foci of white matter 17/48 CF 62 CF 20 h2, 5 CF non-specific finding – Moderate Moderate 18/34 3 4 weeks Transient left Left temporal contusion, Severe Severe weakness DAI 19/46 15 CF 3 days5 CF non-specific finding CF non-specific high signal – No foci of white matter 20/53 15 – – CF non-specific high signal – No foci of white matter 21/41 15 6 days – – Moderate Moderate 22/51 5 3 weeks Transient double vision DAI, cortical Severe Severe 23/24 15 CF 2 weeks2, 5 – – – No 24/29 15 6 days – DAI Mild Moderate 25/28 15 6 weeks Transient anosmia and CF non-specific high signal Moderate Severe visual disturbances foci of white matter 26/16 3 3 weeks Transient double vision, DAI, contusion Mild Severe weakness of left hand, increased left reflexes 27/26 13 5 min, CF 2 weeks5, 7 – Contusion in right Severe Severe cerebellum, DAI 28/54 CF 33 CF 2 weeks3, 5 CF transient – – No symptoms3 29/22 15 20 min, CF 6 days5, 6, 8 – DAI Moderate Moderate 30/34 15 1 h, CF 1 week5, 6, 9 – – Mild Mild 31/19 CF 94 CF 3 weeks4, 5 CF non-specific finding – – No 1Female, 2alcohol, 3respiratory failure, 4electric , 5anaesthesia, sedation, medication, 6hypoxia, 7metabolic disturbance, 8asystole, 9pulmonary thromboembolism with a . GCS: Glasgow Coma Score; PTA: post-traumatic amnesia; DAI: diffuse axonal injury; CF: confounding factors, the variable/finding excluded from the analysis.

J Rehabil Med 39 TBI in patients with SCI 625

Rating Scale (21) were used. Any symptoms of post-traumatic stress estimated to be 40–60% in earlier studies using 1 or 2 TBI disorder (PTSD) (22) and the length of PTA (23) were evaluated ret- indicators (2–7). The higher occurrence of TBI in this study rospectively during the clinical interview by the neuropsychologist. is explained by our combining several sensitive evaluation The neuropsychological examinations were performed 19.6 weeks (mean; SD 11.6) after the injury. Neuropsychological findings with methods. In addition, centre as the only national unit for SCI confounding factors were excluded from the analysis. rehabilitation represents the majority of severe, meaning para- plegic and tetraplegic, traumatic SCI patients in Finland. Severity of TBI Moderate or severe TBI was found in 54.8% of all SCI pa- The diagnostic criteria for classification of TBI severity are outlined tients. Of patients diagnosed with TBI, 73.9% had moderate in Table II. The highest rating of severity received was used to define or severe TBI, which is much higher than the 8–10% typically the severity of TBI of each patient. seen in TBI epidemiological studies (24). The reason for the Statistical analysis high prevalence of moderate and severe TBI in these SCI Descriptive statistics were computed for all relevant variables. A patients is probably the biomechanical effect of high force dependence test was used to examine the dependence between the accidents. A marked as a consequence of moderate neurological level of spinal cord injury and the severity of TBI. or severe TBI is likely, and even after apparently mild TBI more than 30% of patients have been reported to have major problems one year after the injury (24). RESULTS Only 9 patients had received a TBI diagnosis in the acute phase before arrival at the Käpylä Rehabilitation Centre. In Twenty-three of the 31 patients with SCI (74.2%) met one patients with SCI, indicators of TBI, such as LOC and PTA, or more of the diagnostic criteria of TBI (Table III). For 4 of often go unrecognized in acute care and physiatric settings (3). these patients, GCS and PTA could not be reliably defined due The results of neurological and neuroradiological evaluations to confounding factors (use of alcohol at the time of the acci- may be normal despite brain injury (10, 11). Patients with a dent, medication, hypoxia). Two of these 4 patients, however, GCS of 13–15 may also suffer from severe TBI (8, 24). In this showed MRI abnormalities related to TBI, and all 4 patients study, PTA and neuropsychological findings were often found had neuropsychological symptoms or signs due to TBI. Based in patients with absent neurological and neuroradiological on these findings, they were diagnosed with TBI. findings. Only those neuropsychological findings that were Seven (22.6%) patients had a GCS of less than 15, and 19 clinically evaluated to probably be TBI-related were reported (61.3%) had PTA (Table III). Neurological signs or symptoms in the results. Our results suggest that TBI is highly under- due to TBI were found in 4 (12.9%) patients and neuropsy- diagnosed in patients with traumatic SCI. chological signs or symptoms in 21 (67.7%). MRI revealed When all the 5 diagnostic criteria were pooled, TBI was abnormalities specific to TBI in 10 (32.3%) patients. All diagnosed in 74.2% of the patients. Neuropsychological find- non-specific findings or any findings with confounding fac- ing classified the same subgroup of TBI patients respectively tors were excluded from the analysis (Table III). None of the (67.7%). Only 2 patients had PTA but no neuropsychological patients diagnosed for TBI fulfilled the diagnostic criteria for finding. Two patients showed neuropsychological finding due posttraumatic stress disorder or depression. to TBI without any other clear diagnostic criteria findings. In Mild TBI was diagnosed in 6 (19.4%) of the 31 patients. Moder- earlier studies, 40–50% of traumatic SCI patients have had ate TBI was found in 8 (25.8%) and severe in 9 (29.0%) patients cognitive impairments (2, 4, 7). (Tables III and IV). The neurological level of spinal cord injury did Practical problem in diagnosing TBI after SCI, or other not correlate with the presence or severity of TBI (Table IV). severe multi-trauma, is a variety of confounding factors, such as intoxication during the injury, hypoxia, medication, and DISCUSSION complications of physical injuries. The same problem was evident also in this study. In order to avoid false diagnoses, Twenty-three (74.2%) of the 31 patients with SCI were diag- we excluded all the TBI findings with any confounding factors nosed with TBI. The co-occurrence of TBI with SCI has been from the analysis (Table III). Consequently, the actual occur- rence of TBI in patients with traumatic SCI might be even higher than now reported. Table IV. Severity of traumatic brain injury (TBI) according to Diagnosis of TBI in patients with concurrent traumatic neurological level of spinal cord injury SCI influences physiatric care, rehabilitation, and vocational C2-C8 T1–T6 T7– Total planning. To avoid secondary complications, treatment and n % n % n % n % rehabilitation guidelines must be based on knowledge of these patients’ specific cognitive and emotional limitations No TBI 5 33.3 1 12.5 2 25.0 8 25.8 Mild TBI 2 13.3 2 25.0 2 25.0 6 19.4 and needs. Moderate TBI 4 26.7 2 25.0 2 25.0 8 25.8 The full effect of a TBI is often not immediately apparent; the Severe TBI 4 26.7 3 37.5 2 25.0 9 29.0 extent of a mild TBI may go unnoticed for months or even years Total n, % 15 100.0 8 100.0 8 100.0 31 100.0 (25). To assess the significance and long-term consequences of No significant difference was found between groups. a TBI in patients with SCI, a careful follow-up is crucial.

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